ABSTRACT

Major transitions between marine and freshwater habitats are relatively infrequent, primarily as a result of major physiological and ecological challenges. Few species of cartilaginous fish have evolved to occupy freshwater habitats. Current thought suggests that the metabolic physiology of sharks has remained a barrier to the diversification of this taxon in freshwater ecosystems. Here, we demonstrate that the physical properties of water provide an additional constraint for this species-rich group to occupy freshwater systems. Using hydromechanical modeling, we show that occurrence in fresh water results in a two- to three-fold increase in negative buoyancy for sharks and rays. This carries the energetic cost of lift production and results in increased buoyancy-dependent mechanical power requirements for swimming and increased optimal swim speeds. The primary source of buoyancy, the lipid-rich liver, offers only limited compensation for increased negative buoyancy as a result of decreasing water density; maintaining the same submerged weight would involve increasing the liver volume by very large amounts: 3- to 4-fold in scenarios where liver density is also reduced to currently observed minimal levels and 8-fold without any changes in liver density. The first data on body density from two species of elasmobranch occurring in freshwater (the bull shark Carcharhinus leucas, Müller and Henle 1839, and the largetooth sawfish Pristis pristis, Linnaeus 1758) support this hypothesis, showing similar liver sizes as marine forms but lower liver densities, but the greatest negative buoyancies of any elasmobranch studied to date. Our data suggest that the mechanical challenges associated with buoyancy control may have hampered the invasion of freshwater habitats in elasmobranchs, highlighting an additional key factor that may govern the predisposition of marine organisms to successfully establish in freshwater habitats.

FOOTNOTES

Competing interests

The authors declare no competing or financial interests.

Author contributions

A.C.G., D.L.M. and J.A.G. conceived the study. A.C.G., J.J.K., J.M.W. and D.L.M. performed the fieldwork. A.C.G. and J.P. led the data-analysis with contributions from J.A.G. A.C.G., J.P. and J.A.G. drafted the paper with contributions from all other authors.

Funding

This project was generously supported by grants from the Australia Pacific Science Foundation, National Geographic's Waitt Foundation Program, the Fisheries Society of the British Isles and the Western Australian Government's NRM program. A.C.G. was supported by an Endeavour Research Fellowship.

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